Experience-dependent plasticity in S1 caused by noncoincident inputs

Abstract

Prior work has shown that coincident inputs became co-represented in somatic sensory cortex. In this study, the hypothesis that the co-representation of digits required synchronous inputs was tested, and the daily development of two-digit receptive fields was observed with cortical implants. Two adult primates detected temporal differences in tap pairs delivered to two adjacent digits. With stimulus onset asynchronies of > or = 100 ms, representations changed to include two-digit receptive fields across the first 4 wk of training. In addition, receptive fields at sites responsive to the taps enlarged more than twofold, and receptive fields at sites not responsive to the taps had no significant areal change. Further training did not increase the expression of two-digit receptive fields. Cortical responses to the taps were not dependent on the interval length. Stimuli preceding a hit, miss, false positives, and true negatives differed in the ongoing cortical rate from 50 to 100 ms after the stimulus but did not differ in the initial, principal, response to the taps. Response latencies to the emergent responses averaged 4.3 ms longer than old responses, which occurs if plasticity is cortical in origin. New response correlations developed in parallel with the new receptive fields. These data show co-representation can be caused by presentation of stimuli across a longer time window than predicted by spike-timing-dependent plasticity and suggest that increased cortical excitability accompanies new task learning.

FIG. 1

A: implant location. Left: side aspect of the owl monkey brain. Right: anterior. Somatosensory strip in area 3b was implanted. Inset: approximate position of the 49 microelectrode implants in animal 1. Electrodes were implanted across the 2nd (d2), 3rd (d3), and 4th (d4) digital representations on the left hand. B: behavioral task. A trial began with an orienting response, the animal initiating contact with the tips of 2 motors. Then, 2 to 6 standard tap pairs were repeated. After the tap interval changed to the 100-ms target, which was shorter than the standard interval (200 ms), the animal could remove its hand and receive a reward.

FIG. 2

Changes in the maps of somatosensory responses in animal 1. A: drawings of 25 receptive fields as mapped on a day before 2-digit receptive fields emerged. Spatial positions of the outlines of the monkey’s left hand correspond to a 5 × 5 subset of the 49 electrodes of the implant. We surveyed cutaneous (red) and deep (blue) responses as well as responses on the dorsum (green). Gray hands indicate no determinable receptive field from that electrode on the day shown. B: receptive fields 16 days later. Twelve behavioral sessions separated A and B. *Sites where 2-digit receptive fields emerged. Recording sites are arranged in a 350-μm spacing grid. Anterior is right, medial is up.

FIG. 3

Receptive field changes over time. A: receptive field maps from 1 site from 2 wk before the behavior was initiated and 2 wk after. Center plot shows the intersection of all 20 receptive fields. B: normalized receptive field area during training. Receptive field area from each site with a significant tap response was taken from 2 wk before training started to 4 wk after, and each site’s areas were normalized to a within-site mean of 1. Average normalized areas across all sites that responded to the behavioral taps are shown. Areas were significantly larger after training began than before (t-test on normalized areas, P < 10⁻⁷). Areas without significant tap responses had insignificant areal changes before and after behavioral initiation.

FIG. 4

Emergence of 2-digit receptive fields. A: sampled single-unit responses on 1 microelectrode in animal 1 over a 4-day period in which 2-digit responses emerged. Responses were defined across all 100-ms tap intervals delivered during the hold. A site had 2-digit responses if there were significant increments in firing rate, measured in action potentials per second, between 10 and 40 ms after a digit was tapped, relative to pretap activity. Gray bars indicate time that taps were delivered. B: sampled multiunit responses over 3 wk from 1 electrode in animal 2 showing the emergence of 2-digit receptive fields in the 3rd week.

FIG. 5

A: cumulative plot of the percentage of sites that had 2-digit response properties. Thick line, development of 2-digit responses in 4 of 11 sites in animal 2; thin line, development of such responses in 4 of 10 sites in animal 1. Total number of sites used in plot includes all electrodes that sampled responses to either tap in any behavioral session. B: 2-digit receptive field development does not depend on order of taps. Same data as in A replotted to show sites that initially only responded to the 1st tap delivered to the index finger tip, but finally, after behavioral training, also had an emergen response to the 2nd tap at a different finger (thick line). Conversely, we also found sites that initially responded only to the 2nd tap, but finally had an emergent response to the 1st tap (thin line). C: population activity in animal 1. Sum of all sampled activity in response to target stimulus. Tap at time 0 occurred on digit 2, and tap at time 100 occurred on digit 3. D: population activity in animal 2. Tap at time 0 occurred on digit 2, and tap at time 100 occurred on digit 1.

FIG. 6

Response latencies. Peristimulus time histograms (PSTHs) show responses to the 1st (Tap 1) and 2nd taps (Tap 2); taps (gray bars) and responses are aligned in time to allow for a better comparison of latencies. We compared responses that are present initially (solid lines) to emergent responses (dashed lines). A: example site in which latencies of the preexisting (solid) and the emergent (dashed) tap responses were identical. Before behavioral training, responses were sampled only to the 1st tap. B: example site in which latency of the emergent response (dashed) was about 5 ms longer than latency of the preexisting response (solid).

FIG. 7

Responses to different behavioral categories of trials. A: PSTH sum of all neuronal responses to the 1st 2 presentations of the target stimuli on hit and miss trials. B: PSTH sum of all neuronal responses, on a different day, to stimuli preceding false-positive and true-negative behavioral responses.

FIG. 8

Responses do not depend on the tap intervals. A: firing rate histograms of responses from neurons at a 2-digit site to taps at 100- and 200-ms intervals. B: population data showing strength of all significant neural responses to 2nd taps of 200-ms intervals compared with responses to 2nd taps of 100-ms intervals. No significant effects of interval length on response to 2nd taps were found using sign or t-test. Stars, data from animal 1; circles, data from animal 2; line, prediction if the 2 responses are equal. Each data point shows integral of response PSTH after subtracting prestimulus rate for the 2 conditions. This number is averaged over all daily trials.

FIG. 9

Spike correlations. A: cutaneous spiking receptive fields from sites X and Y in animal 1. Distance between microelectrodes is 1.26 mm. Light-shaded receptive field was measured at site Y; dark-shaded receptive field was measured at the tip of d2 was measured at site X. Cross-hatched receptive field is shared. B: cross-correlation between X and Y during tap on index finger. Thin line, independent prediction; thick line, actual covariation; dashed line. single bin significance threshold for P < 0.0003. Elevated covariation at time 0 is significant for fine spike timing correlations. C: spatial distribution of cell assembly correlations in both animals. In the 1st 3 training session (thin line) there were fewer correlated pairs than in the last 3 training sessions (thick line).